Histone 3 lysine 4 monomethylation supports activation of transcription in S. cerevisiae during nutrient stress
Tóm tắt
Mono-methylation of the fourth lysine on the N-terminal tail of histone H3 was found to support the induction of RNA polymerase II transcription in S. cerevisiae during nutrient stress. In S. cerevisiae, the mono-, di- and tri-methylation of lysine 4 on histone H3 (H3K4) is catalyzed by the protein methyltransferase, Set1. The three distinct methyl marks on H3K4 act in discrete ways to regulate transcription. Nucleosomes enriched with tri-methylated H3K4 are usually associated with active transcription whereas di-methylated H3K4 is associated with gene repression. Mono-methylated H3K4 has been shown to repress gene expression in S. cerevisiae and is detected at enhancers and promoters in eukaryotes. S. cerevisiae set1Δ mutants unable to methylate H3K4 exhibit growth defects during histidine starvation. The growth defects are rescued by either a wild-type allele of SET1 or partial-function alleles of set1, including a mutant that predominantly generates H3K4me1 and not H3K4me3. Rescue of the growth defect is associated with induction of the HIS3 gene. Growth defects observed when set1Δ cultures were starved for isoleucine and valine were also rescued by wild-type SET1 or partial-function set1 alleles. The results show that H3K4me1, in the absence of H3K4me3, supports transcription of the HIS3 gene and expression of one or more of the genes required for biosynthesis of isoleucine and valine during nutrient stress. Set1-like methyltransferases are evolutionarily conserved, and research has linked their functions to developmental gene regulation and several cancers in higher eukaryotes. Identification of mechanisms of H3K4me1-mediated activation of transcription in budding yeast will provide insight into gene regulation in all eukaryotes.
Tài liệu tham khảo
Allaire J (2012) RStudio: integrated development environment for R. Boston 537:538
Bae S, Lesch BJ (2020) H3K4me1 distribution predicts transcription state and poising at promoters. Front Cell Dev Biol 8:289
Bae HJ, Dubarry M, Jeon J, Soares LM, Dargemont C, Kim J, Geli V, Buratowski S (2020) The Set1 N-terminal domain and Swd2 interact with RNA polymerase II CTD to recruit COMPASS. Nat Commun 11:2181. https://doi.org/10.1038/s41467-020-16082-2
Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ, McMahon S, Karlsson EK, Kulbokas EJ, Gingeras TR, Schreiber SL, Lander ES (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120:169–181. https://doi.org/10.1016/j.cell.2005.01.001
Breen TR (1999) Mutant alleles of the Drosophila trithorax gene produce common and unusual homeotic and other developmental phenotypes. Genetics 152:319–344
Brennan MB, Struhl K (1980) Mechanisms of increasing expression of a yeast gene in Escherichia coli. J Mol Biol 136:333–338. https://doi.org/10.1016/0022-2836(80)90377-0
Briggs SD, Bryk M, Strahl BD, Cheung WL, Davie JK, Dent SY, Winston F, Allis CD (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 15:3286–3295. https://doi.org/10.1101/gad.940201
Bryk M, Briggs SD, Strahl BD, Curcio MJ, Allis CD, Winston F (2002) Evidence that Set1, a factor required for methylation of histone H3, regulates rDNA silencing in S. cerevisiae by a Sir2-independent mechanism. Curr Biol 12:165–170. https://doi.org/10.1016/S0960-9822(01)00652-2
Calo E, Wysocka J (2013) Modification of enhancer chromatin: what, how, and why? Mol Cell 49:825–837. https://doi.org/10.1016/j.molcel.2013.01.038
Carvin CD, Kladde MP (2004) Effectors of lysine 4 methylation of histone H3 in Saccharomyces cerevisiae are negative regulators of PHO5 and GAL1-10. J Biol Chem 279:33057–33062. https://doi.org/10.1074/jbc.M405033200
Castillo J, López-Rodas G, Franco L (2017) Histone post-translational modifications and nucleosome organisation in transcriptional regulation: some open questions. In: Atassi MZ (ed) Protein reviews, vol 18. Springer Singapore, Singapore, pp 65–92
Catarino RR, Stark A (2018) Assessing sufficiency and necessity of enhancer activities for gene expression and the mechanisms of transcription activation. Genes Dev 32:202–223. https://doi.org/10.1101/gad.310367.117
Cenik BK, Shilatifard A (2021) COMPASS and SWI/SNF complexes in development and disease. Nat Rev Genet 22:38–58. https://doi.org/10.1038/s41576-020-0278-0
Chatterjee N, Sinha D, Lemma-Dechassa M, Tan S, Shogren-Knaak MA, Bartholomew B (2011) Histone H3 tail acetylation modulates ATP-dependent remodeling through multiple mechanisms. Nucleic Acids Res 39:8378–8391. https://doi.org/10.1093/nar/gkr535
Cheng J, Blum R, Bowman C, Hu D, Shilatifard A, Shen S, Dynlacht BD (2014) A role for H3K4 monomethylation in gene repression and partitioning of chromatin readers. Mol Cell 53:979–992. https://doi.org/10.1016/j.molcel.2014.02.032
Clark-Adams CD, Norris D, Osley MA, Fassler JS, Winston F (1988) Changes in histone gene dosage alter transcription in yeast. Genes Dev 2:150–159
Côté J, Peterson CL, Workman JL (1998) Perturbation of nucleosome core structure by the SWI/SNF complex persists after its detachment, enhancing subsequent transcription factor binding. Proc Natl Acad Sci USA 95:4947–4952. https://doi.org/10.1073/pnas.95.9.4947
Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, Boyer LA, Young RA, Jaenisch R (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci USA 107:21931–21936. https://doi.org/10.1073/pnas.1016071107
Dillon SC, Zhang X, Trievel RC, Cheng X (2005) The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 6:227. https://doi.org/10.1186/gb-2005-6-8-227
Dorighi KM, Swigut T, Henriques T, Bhanu NV, Scruggs BS, Nady N, Still CD 2nd, Garcia BA, Adelman K, Wysocka J (2017) Mll3 and Mll4 facilitate enhancer RNA synthesis and transcription from promoters independently of H3K4 monomethylation. Mol Cell 66:568-576.e564. https://doi.org/10.1016/j.molcel.2017.04.018
Falco SC, Dumas KS (1985) Genetic analysis of mutants of Saccharomyces cerevisiae resistant to the herbicide sulfometuron methyl. Genetics 109:21–35. https://doi.org/10.1093/genetics/109.1.21
Falco SC, Dumas KS, Livak KJ (1985) Nucleotide sequence of the yeast ILV2 gene which encodes acetolactate synthase. Nucleic Acids Res 13:4011–4027. https://doi.org/10.1093/nar/13.11.4011
Fink GR (1964) Gene-enzyme relations in histidine biosynthesis in yeast. Science 146:525. https://doi.org/10.1126/science.146.3643.525
Froimchuk E, Jang Y, Ge K (2017) Histone H3 lysine 4 methyltransferase KMT2D. Gene 627:337–342. https://doi.org/10.1016/j.gene.2017.06.056
Ginsburg DS, Govind CK, Hinnebusch AG (2009) NuA4 lysine acetyltransferase Esa1 is targeted to coding regions and stimulates transcription elongation with Gcn5. Mol Cell Biol 29:6473–6487. https://doi.org/10.1128/MCB.01033-09
Han M, Grunstein M (1988) Nucleosome loss activates yeast downstream promoters in vivo. Cell 55:1137–1145. https://doi.org/10.1016/0092-8674(88)90258-9
Hill DE, Hope IA, Macke JP, Struhl K (1986) Saturation mutagenesis of the yeast his3 regulatory site: requirements for transcriptional induction and for binding by GCN4 activator protein. Science 234:451
Hinnebusch AG (2005) Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 59:407–450. https://doi.org/10.1146/annurev.micro.59.031805.133833
Hope IA, Struhl K (1985) GCN4 protein, synthesize in vitro, binds HIS3 regulatory sequences: implications for general control of amino acid biosynthetic genes in yeast. Cell 43:177–188. https://doi.org/10.1016/0092-8674(85)90022-4
Hyun K, Jeon J, Park K, Kim J (2017) Writing, erasing and reading histone lysine methylations. Exp Mol Med 49:e324–e324. https://doi.org/10.1038/emm.2017.11
Izban MG, Luse DS (1992) Factor-stimulated RNA polymerase II transcribes at physiological elongation rates on naked DNA but very poorly on chromatin templates. J Biol Chem 267:13647–13655
Jeong KW, Kim K, Situ AJ, Ulmer TS, An W, Stallcup MR (2011) Recognition of enhancer element-specific histone methylation by TIP60 in transcriptional activation. Nat Struct Mol Biol 18:1358–1365. https://doi.org/10.1038/nsmb.2153
Jiang D, Kong NC, Gu X, Li Z, He Y (2011) Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet 7:e1001330. https://doi.org/10.1371/journal.pgen.1001330
Kandoth C, McLellan MD, Vandin F, Ye K, Niu B, Lu C, Xie M, Zhang Q, McMichael JF, Wyczalkowski MA, Leiserson MDM, Miller CA, Welch JS, Walter MJ, Wendl MC, Ley TJ, Wilson RK, Raphael BJ, Ding L (2013) Mutational landscape and significance across 12 major cancer types. Nature 502:333. https://doi.org/10.1038/nature12634. https://www.nature.com/articles/nature12634#supplementary-information
Kang Y, Kim YW, Kang J, Kim A (2021) Histone H3K4me1 and H3K27ac play roles in nucleosome eviction and eRNA transcription, respectively, at enhancers. FASEB J 35:e21781. https://doi.org/10.1096/fj.202100488R
Kim T, Buratowski S (2009) Dimethylation of H3K4 by Set1 recruits the Set3 histone deacetylase complex to 5′ transcribed regions. Cell 137:259–272. https://doi.org/10.1016/j.cell.2009.02.045
Kornberg RD, Thonmas JO (1974) Chromatin structure: oligomers of the histones. Science 184:865. https://doi.org/10.1126/science.184.4139.865
Krogan NJ, Dover J, Khorrami S, Greenblatt JF, Schneider J, Johnston M, Shilatifard A (2002) COMPASS, a histone H3 (lysine 4) methyltransferase required for telomeric silencing of gene expression. J Biol Chem 277:10753–10755
Kuo M-H, Allis CD (1998) Roles of histone acetyltransferases and deacetylases in gene regulation. BioEssays 20:615–626. https://doi.org/10.1002/(SICI)1521-1878(199808)20:8%3c615::AID-BIES4%3e3.0.CO;2-H
Kuo M-H, vom Baur E, Struhl K, Allis CD (2000) Gcn4 activator targets Gcn5 histone acetyltransferase to specific promoters independently of transcription. Mol Cell 6:1309–1320. https://doi.org/10.1016/S1097-2765(00)00129-5
Kusch T (2012) Histone H3 lysine 4 methylation revisited. Transcription 3:310–314. https://doi.org/10.4161/trns.21911
Latham JA, Chosed RJ, Wang S, Dent SY (2011) Chromatin signaling to kinetochores: transregulation of Dam1 methylation by histone H2B ubiquitination. Cell 146:709–719. https://doi.org/10.1016/j.cell.2011.07.025
Lee DY, Hayes JJ, Pruss D, Wolffe AP (1993) A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 72:73–84. https://doi.org/10.1016/0092-8674(93)90051-Q
Lee J-S, Shukla A, Schneider J, Swanson SK, Washburn MP, Florens L, Bhaumik SR, Shilatifard A (2007) Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131:1084–1096. https://doi.org/10.1016/j.cell.2007.09.046
Lee KY, Chen Z, Jiang R, Meneghini MD (2018) H3K4 methylation dependent and independent chromatin regulation by JHD2 and SET1 in budding yeast. G3 (bethesda, Md) 8:1829–1839. https://doi.org/10.1534/g3.118.200151
Li C, Mueller JE, Bryk M (2006) Sir2 represses endogenous polymerase II transcription units in the ribosomal DNA nontranscribed spacer. Mol Biol Cell 17:3848–3859. https://doi.org/10.1091/mbc.e06-03-0205
Liu CL, Kaplan T, Kim M, Buratowski S, Schreiber SL, Friedman N, Rando OJ (2005) Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol 3:e328. https://doi.org/10.1371/journal.pbio.0030328
Local A, Huang H, Albuquerque CP, Singh N, Lee AY, Wang W, Wang C, Hsia JE, Shiau AK, Ge K, Corbett KD, Wang D, Zhou H, Ren B (2018) Identification of H3K4me1-associated proteins at mammalian enhancers. Nat Genet 50:73–82. https://doi.org/10.1038/s41588-017-0015-6
Miller T, Krogan NJ, Dover J, Erdjument-Bromage H, Tempst P, Johnston M, Greenblatt JF, Shilatifard A (2001) COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc Natl Acad Sci USA 98:12902–12907. https://doi.org/10.1073/pnas.231473398
Morillon A, Karabetsou N, Nair A, Mellor J (2005) Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol Cell 18:723–734. https://doi.org/10.1016/j.molcel.2005.05.009
Mueller JE, Canze M, Bryk M (2006) The requirements for COMPASS and Paf1 in transcriptional silencing and methylation of histone H3 in Saccharomyces cerevisiae. Genetics 173:557–567. https://doi.org/10.1534/genetics.106.055400
Musselman CA, Lalonde M-E, Côté J, Kutateladze TG (2012) Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol 19:1218–1227. https://doi.org/10.1038/nsmb.2436
Nadal-Ribelles M, Mas G, Millán-Zambrano G, Solé C, Ammerer G, Chávez S, Posas F, de Nadal E (2015) H3K4 monomethylation dictates nucleosome dynamics and chromatin remodeling at stress-responsive genes. Nucleic Acids Res 43:4937–4949. https://doi.org/10.1093/nar/gkv220
Nagy PL, Griesenbeck J, Kornberg RD, Cleary ML (2002) A trithorax-group complex purified from Saccharomyces cerevisiae is required for methylation of histone H3. Proc Natl Acad Sci USA 99:90–94. https://doi.org/10.1073/pnas.221596698
Natarajan K, Jackson BM, Zhou H, Winston F, Hinnebusch AG (1999) Transcriptional activation by Gcn4p involves independent interactions with the SWI/SNF complex and the SRB/mediator. Mol Cell 4:657–664. https://doi.org/10.1016/S1097-2765(00)80217-8
Ng HH, Robert F, Young RA, Struhl K (2003) Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11:709–719. https://doi.org/10.1016/S1097-2765(03)00092-3
Nislow C, Ray E, Pillus L (1997) SET1, a yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Mol Biol Cell 8:2421–2436. https://doi.org/10.1091/mbc.8.12.2421
Pinskaya M, Morillon A (2009) Histone H3 lysine 4 di-methylation: a novel mark for transcriptional fidelity? Epigenetics 4:302–306
Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, Bell GW, Walker K, Rolfe PA, Herbolsheimer E, Zeitlinger J, Lewitter F, Gifford DK, Young RA (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122:517–527. https://doi.org/10.1016/j.cell.2005.06.026
Pray-Grant MG, Daniel JA, Schieltz D, Yates JR, Grant PA (2005) Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 433:434–438. https://doi.org/10.1038/nature03242
Qu Q, Takahashi Y-h, Yang Y, Hu H, Zhang Y, Brunzelle JS, Couture J-F, Shilatifard A, Skiniotis G (2018) Structure and conformational dynamics of a COMPASS histone H3K4 methyltransferase complex. Cell 174:1117-1126.e1112. https://doi.org/10.1016/j.cell.2018.07.020
Ramakrishnan S, Pokhrel S, Palani S, Pflueger C, Parnell TJ, Cairns BR, Bhaskara S, Chandrasekharan MB (2016) Counteracting H3K4 methylation modulators Set1 and Jhd2 co-regulate chromatin dynamics and gene transcription. Nat Commun 7:11949. https://doi.org/10.1038/ncomms11949
Rickels R, Herz H-M, Sze CC, Cao K, Morgan MA, Collings CK, Gause M, Takahashi Y-H, Wang L, Rendleman EJ, Marshall SA, Krueger A, Bartom ET, Piunti A, Smith ER, Abshiru NA, Kelleher NL, Dorsett D, Shilatifard A (2017) Histone H3K4 monomethylation catalyzed by Trr and mammalian COMPASS-like proteins at enhancers is dispensable for development and viability. Nat Genet 49:1647–1653. https://doi.org/10.1038/ng.3965
Roguev A, Schaft D, Shevchenko A, Pijnappel WW, Wilm M, Aasland R, Stewart AF (2001) The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J 20:7137–7148. https://doi.org/10.1093/emboj/20.24.7137
Rose MD, Winston F, Hieter P (1990) Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
Ruault M, Brun ME, Ventura M, Roizès G, De Sario A (2002) MLL3, a new human member of the TRX/MLL gene family, maps to 7q36, a chromosome region frequently deleted in myeloid leukaemia. Gene 284:73–81. https://doi.org/10.1016/S0378-1119(02)00392-X
Santos-Rosa H, Schneider R, Bernstein BE, Karabetsou N, Morillon A, Weise C, Schreiber SL, Mellor J, Kouzarides T (2003) Methylation of histone H3 K4 mediates association of the Isw1p ATPase with chromatin. Mol Cell 12:1325–1332. https://doi.org/10.1016/S1097-2765(03)00438-6
Schmitt ME, Brown TA, Trumpower BL (1990) A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res 18:3091–3092. https://doi.org/10.1093/nar/18.10.3091
Schneider J, Wood A, Lee J-S, Schuster R, Dueker J, Maguire C, Swanson SK, Florens L, Washburn MP, Shilatifard A (2005) Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell 19:849–856. https://doi.org/10.1016/j.molcel.2005.07.024
Schrodinger, LLC (2015) The PyMOL molecular graphics system, version 1.8
Sharifi-Zarchi A, Gerovska D, Adachi K, Totonchi M, Pezeshk H, Taft RJ, Scholer HR, Chitsaz H, Sadeghi M, Baharvand H, Arauzo-Bravo MJ (2017) DNA methylation regulates discrimination of enhancers from promoters through a H3K4me1-H3K4me3 seesaw mechanism. BMC Genomics 18:964. https://doi.org/10.1186/s12864-017-4353-7
Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Peña P, Lan F, Kaadige MR, Lacoste N, Cayrou C, Davrazou F, Saha A, Cairns BR, Ayer DE, Kutateladze TG, Shi Y, Côté J, Chua KF, Gozani O (2006) ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442:96–99. https://doi.org/10.1038/nature04835
Shilatifard A (2012) The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu Rev Biochem 81:65–95. https://doi.org/10.1146/annurev-biochem-051710-134100
Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27
Slany RK (2009) The molecular biology of mixed lineage leukemia. Haematologica 94:984–993. https://doi.org/10.3324/haematol.2008.002436
Soares LM, He PC, Chun Y, Suh H, Kim T, Buratowski S (2017) Determinants of histone H3K4 methylation patterns. Mol Cell 68(773–785):e776. https://doi.org/10.1016/j.molcel.2017.10.013
Sollier J, Lin W, Soustelle C, Suhre K, Nicolas A, Géli V, de La Roche S-A (2004) Set1 is required for meiotic S-phase onset, double-strand break formation and middle gene expression. EMBO J 23:1957–1967. https://doi.org/10.1038/sj.emboj.7600204
Swanson MS, Malone EA, Winston F (1991) SPT5, an essential gene important for normal transcription in Saccharomyces cerevisiae, encodes an acidic nuclear protein with a carboxy-terminal repeat. Mol Cell Biol 11:3009–3019. https://doi.org/10.1128/mcb.11.6.3009
Swanson MJ, Qiu H, Sumibcay L, Krueger A, Kim S-j, Natarajan K, Yoon S, Hinnebusch AG (2003) A multiplicity of coactivators is required by Gcn4p at individual promoters in vivo. Mol Cell Biol 23:2800–2820. https://doi.org/10.1128/mcb.23.8.2800-2820.2003
Takahashi Y-h, Westfield GH, Oleskie AN, Trievel RC, Shilatifard A, Skiniotis G (2011) Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human. Proc Natl Acad Sci USA 108:20526–20531. https://doi.org/10.1073/pnas.1109360108
Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H, Li H, Baker L, Boyle J, Blair LP, Chait Brian T, Patel DJ, Aitchison JD, Tackett AJ, Allis CD (2006) Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol Cell 24:785–796. https://doi.org/10.1016/j.molcel.2006.10.026
Vermeulen M, Mulder KW, Denissov S, Pijnappel WWMP, van Schaik FMA, Varier RA, Baltissen MPA, Stunnenberg HG, Mann M, Timmers HTM (2007) Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131:58–69. https://doi.org/10.1016/j.cell.2007.08.016
Wang Y, Ding Z, Liu X, Bao Y, Huang M, Wong CCL, Hong X, Cong Y (2018) Architecture and subunit arrangement of the complete Saccharomyces cerevisiae COMPASS complex. Sci Rep 8:17405. https://doi.org/10.1038/s41598-018-35609-8
Wasylyk B, Chambon P (1979) Transcription by eukaryotic RNA polymerases A and B of chromatin assembled in vitro. Eur J Biochem 98:317–327. https://doi.org/10.1111/j.1432-1033.1979.tb13191.x
Weiner A, Chen HV, Liu CL, Rahat A, Klien A, Soares L, Gudipati M, Pfeffner J, Regev A, Buratowski S, Pleiss JA, Friedman N, Rando OJ (2012) Systematic dissection of roles for chromatin regulators in a yeast stress response. PLoS Biol 10:e1001369. https://doi.org/10.1371/journal.pbio.1001369
Williamson K, Schneider V, Jordan RA, Mueller JE, Pozzi MH, Bryk M (2013) Catalytic and functional roles of conserved amino acids in the SET domain of the S. cerevisiae lysine methyltransferase Set1. PLoS ONE 8:e57974
Workman JL, Kingston RE (1998) Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem 67:545–579. https://doi.org/10.1146/annurev.biochem.67.1.545
Wyrick JJ, Holstege FC, Jennings EG, Causton HC, Shore D, Grunstein M, Lander ES, Young RA (1999) Chromosomal landscape of nucleosome-dependent gene expression and silencing in yeast. Nature 402:418–421. https://doi.org/10.1038/46567
Yan J, Chen S-AA, Local A, Liu T, Qiu Y, Dorighi KM, Preissl S, Rivera CM, Wang C, Ye Z, Ge K, Hu M, Wysocka J, Ren B (2018) Histone H3 lysine 4 monomethylation modulates long-range chromatin interactions at enhancers. Cell Res 28:204–220. https://doi.org/10.1038/cr.2018.1
Yu R, Sun L, Sun Y, Han X, Qin L, Dang W (2019) Cellular response to moderate chromatin architectural defects promotes longevity. Sci Adv 5:eaav1165. https://doi.org/10.1126/sciadv.aav1165
Zhang K, Lin W, Latham JA, Riefler GM, Schumacher JM, Chan C, Tatchell K, Hawke DH, Kobayashi R, Dent SY (2005) The Set1 methyltransferase opposes Ipl1 aurora kinase functions in chromosome segregation. Cell 122:723–734. https://doi.org/10.1016/j.cell.2005.06.021